Forest Ecology and Management 289 (2013) 98–105

Contents lists available at SciVerse ScienceDirect

Forest Ecology and Management

journal homepage: www.elsevier .com/ locate/ foreco

Regeneration responses to exogenous disturbance gradients in southernAppalachian Picea-Abies forests

Sarah E. Stehn a,b, Michael A. Jenkins c,⇑, Christopher R. Webster a, Shibu Jose d

a School of Forest Resources and Environmental Science, Michigan Technological University, 1400 Townsend Drive, Houghton, MI 49931, United Statesb Denali National Park and Preserve and Central Alaska Network, National Park Service, P.O. Box 9, Denali Park, AK 99755, United Statesc Department of Forestry and Natural Resources, Purdue University, 715 West State Street, West Lafayette, IN 47907, United Statesd School of Natural Resources, University of Missouri, 203 Anheuser-Busch Natural Resources Building, Columbia, MO 65211, United States

a r t i c l e i n f o a b s t r a c t

Article history:Received 5 July 2012Received in revised form 21 September 2012Accepted 24 September 2012Available online 28 November 2012

Keywords:Forest regenerationInvasive insectsSoil chemistryTree mortalityPatch dynamicsGreat Smoky Mountains National Park

0378-1127/$ - see front matter � 2012 Elsevier B.V. Ahttp://dx.doi.org/10.1016/j.foreco.2012.09.034

⇑ Corresponding author. Tel.: +1 765 494 3602; faxE-mail addresses: sarah_stehn@nps.gov (S.E. Stehn)

Jenkins), cwebster@mtu.edu (C.R. Webster), joses@mi

Because of the devastation caused by the combined impacts of the balsam woolly adelgid (Adelges piceae;BWA, a non-native insect) and chronic acid deposition, Picea-Abies (spruce-fir) forests are one of the mostthreatened vegetation communities in North America. Endemic Abies fraseri (Fraser fir), the dominantoverstory species in these forests, has experienced near complete overstory mortality as result of theadelgid. Observed forest regeneration patterns suggest high spatial variability, with dense patches ofRubus spp. (blackberry), A. fraseri, and deciduous regeneration repeating across the landscape. To quantifythe spatial variability and density of A. fraseri, Picea rubens (red spruce), and deciduous regeneration inthese forests, we sampled 60 randomly selected plots within Picea-Abies forests of Great Smoky Moun-tains National Park (GSMNP). As a measure of local variability in regeneration, we used regeneration den-sity within 30 1 � 1 m subplots per plot to calculate a coefficient of within-plot variation for each species.Despite the impacts of the BWA and chronic acid deposition, A. fraseri remained an important componentof southern Appalachian Picea-Abies forests at elevations above 1750 m. Density of A. fraseri in all sizeclasses was associated with time since disturbance by BWA infestation. On plots where A. fraseri regen-eration occurred, its local variability (among 30 subplots) was significantly greater than that of P. rubensor deciduous species. Regression models attributed this local-scale variability in A. fraseri regeneration tothe influence of elevation, Rubus spp. cover, B-horizon nitrogen concentration, and O-horizon calcium toaluminum ratio. We propose that co-occurring gradients of BWA-induced mortality and acid depositionhave created patches of increased light and nitrogen availability, which have increased competition fromruderal species such as Rubus spp. Additionally, our results suggest that high soil aluminum content rel-ative to calcium may exclude A. fraseri from certain locations, further contributing to the local variabilityof A. fraseri regeneration.

� 2012 Elsevier B.V. All rights reserved.

1. Introduction

Complexity in ecosystems increases resilience by increasing thecapability of a system to absorb the effects of disturbance withoutsevere alterations to function (Nystrom and Folke, 2001; Bengts-son, 2002). However, even in complex systems exogenous distur-bance and species loss can quickly degrade ecological resilience,leading towards shifts to alternate stable states (Gunderson,2000; Folke et al., 2004). Faced with two such exogenous distur-bances over the past 30 years, a non-native insect infestation andchronic acid deposition (White, 1984b), Picea rubens-Abies fraseri(red spruce-Fraser fir) forests of the southern Appalachians are atrisk of a decline in ecological resilience. The balsam woolly adelgid

ll rights reserved.

: +1 765 494 9461., jenkinma@purdue.edu (M.A.ssouri.edu (S. Jose).

(BWA; Adelges piceae), an insect native to Europe, has decimatedmature A. fraseri throughout the Region. First noted in 1957(Speers, 1958), the BWA occurred throughout all southern Appala-chian P. rubens-A. fraseri stands by the late 1980s (Eagar, 1984). Thepre-infestation density of mature A. fraseri, combined with thetime interval since infestation, have created a variety of contempo-rary overstory conditions (Smith and Nicholas, 1998), resulting inconsiderable variation in stand microclimate throughout the Pi-cea-Abies forest zone (White, 1984a). Because the importance ofA. fraseri increases with elevation, the severity of BWA-inducedmortality and resulting effects on forest structure also increasewith elevation. In addition, the poorly-buffered and highly-weath-ered soils of these forests receive some of the highest rates of aciddeposition in North America (Weathers et al., 2006).

Although legislation has led to decreased deposition rates(Shaver et al., 1994), critical load calculations for GSMNP indicatethat an additional 53% reduction in S and N inputs is required to

S.E. Stehn et al. / Forest Ecology and Management 289 (2013) 98–105 99

protect high-elevation Picea-Abies forests from the effects of acidi-fication and an 89% reduction is required to protect forests fromthe effects of N saturation (Pardo and Duarte, 2007). Long-termsaturation continues to affect soil chemistry and vegetation(Watmough et al., 2005) by reducing the availability of soil cations(Peterjohn et al., 1996; Robarge and Johnson, 1992; Adams et al.,2007) and mobilizing elemental aluminum (Johnson et al., 1991;Lawrence et al., 1995; Elias et al., 2009), which is highly toxic toplants. Implicated in the decline of P. rubens, high levels ofaluminum relative to calcium cause reduced growth andincreased vulnerability to extant secondary diseases and insectpests (Shortle and Smith, 1988; McLaughlin et al., 1990; Shortleet al., 1997).

The establishment of new cohorts following exogenous distur-bance is critical to the maintenance of ecological resilience inforests. The abundance and spatial distribution of woody regen-eration at landscape and regional scales are principally deter-mined by environmental gradients, particularly climatic, whichgreatly influence the ability of a species to establish and persist(Ohmann and Spies, 1998). At more local scales, the spatial com-plexity of woody regeneration is enhanced by recurrent distur-bances, such as ice storms (Nicholas and Zedaker, 1989) orwind events (Rich et al., 2007), that vary in severity across envi-ronmental gradients (Everham and Brokaw, 1996) and result inindividualistic responses by species (Levin, 2000). Site historyinfluences the response of communities to contemporary distur-bance, which contributes to structural and compositional charac-teristics that buffer or amplify the effects of subsequentdisturbance (e.g., Foster et al., 1992). Additionally, chronic stressmay reduce the vigor of particular species in post-disturbancecommunities, contributing to varied successional patterns andtrajectories through altered regeneration dynamics (Zvereva andKozlov, 2001).

Within the Picea-Abies forest zone of the southern AppalachianMountains, regeneration of the dominant species is highly variableand reflects the post-adelgid patchiness of the overstory vegetation(Allen and Kupfer, 2001). As an endemic species, the survival andregeneration of A. fraseri is of particular interest, and lack of viableseed (Nicholas et al., 1992) and competition with Rubus spp.(Pauley, 1989; Pauley and Clebsch, 1990) have been offered aspotential drivers of decline. Future A. fraseri populations in thesouthern Appalachians will likely consist of decreasing numbersof even-aged patches in varied stages of regeneration and mortalityfollowing recurrent outbreaks of BWA (Eagar, 1984; Smith andNicholas, 2000).

While the effects of BWA-induced disturbance on forest compo-sition and structure are well documented, the effects of edaphiccharacteristics influenced by acid deposition have received lessstudy. Past research into the concurrent effects of acid depositionand BWA infestation has typically focused on the overstory (Hainand Arthur, 1985; Hollingsworth and Hain, 1991, 1994; Lee et al.,1997; but see Stehn et al., 2011). In other forest types, acid depo-sition has been shown to influence the competitive dynamics ofground-layer vegetation (Bobbink et al., 1998; Gilliam, 2006),including woody regeneration (Blake and Goulding, 2002; Zaccherioand Finzi, 2007). To examine how edaphic characteristics interactwith disturbance to influence tree regeneration dynamics andspatial patterning, we sampled vegetation and soils across 60 plotsin Picea-Abies forests of the southern Appalachian Mountains. Wehypothesized that concurrent effects of acid deposition andBWA-induced disturbance influence competitive dynamics ofground-layer vegetation in these forests, leading to local spatialvariability in species composition and abundance of woodyregeneration.

2. Methods

2.1. Study sites

Our study sites were located within Picea-Abies forests of GreatSmoky Mountains National Park (GSMNP; 35�350 N, 83�280 W),which is the dominant forest type above 1550 m in the southernAppalachians. Sixty plots were randomly selected from a stratifica-tion of modeled acid deposition (Weathers et al., 2006) and over-story vegetation type using the stratified random point functionof Hawth’s Analysis Tools for ArcGIS (Version 2.10). Because mod-eled sulfur deposition in the Picea-Abies zone ranges from 5 to42 kg sulfur ha�1 yr�1, we attempted to capture the existing natu-ral gradient by selecting 15 plots in each of four deposition catego-ries (6–14.99, 15–23.99, 24–32.99, 33–42 kg sulfur ha�1 yr�1). Tolimit our sampling to the Picea-Abies zone, plot locations were lim-ited to the Appalachian Highlands High Elevation Spruce-fir ForestsEcological Group as defined by NatureServe (White et al., 2003). A.fraseri dominated 40 plots, ten in each acid deposition category,and P. rubens dominated 20 plots, five in each acid deposition cat-egory. For reasonable accessibility, plots were constrained to loca-tions greater than 30 m, but less than or equal to 500 m from anyroad or trail, and to slopes of less than 80% grade. We sampled 33plots in 2007 and 27 plots in 2008.

2.2. Field methods

We measured woody regeneration in multiple size classesacross all sixty plots. Within each 20 � 20 m plot, ground layervegetation was sampled in three 20 m line transects. Transectswere equally spaced across the plot and placed parallel to the con-tour of the slope. In 10 1 � 1 m square subplots upslope of eachtransect, we tallied seedlings and small sapling regeneration<137 cm in height by species into three height classes (<10 cm,10–50 cm, and 50–137 cm), cumulatively referred to as smallregeneration. In two 10 � 10 m quadrants of each plot, we counteddensity of medium (0.1–5 cm dbh) and large (5–10 cm dbh) regen-eration. We recorded the diameter of all tree (P10 cm diameter atbreast height, dbh) by species across the entire 20 � 20 m plot.Linear cover of coarse woody debris by decay class (Jenkins et al.,2004) was estimated along each 20 m transect (100 � [linear coverintercepted/total transect length (3 � 20 = 60)]).

Due to the tendency of Rubus spp. and Rhododendron spp. L. toform dense patches of small stems, we quantified overall cover ofthese species by visually estimating percent cover by class (0–1%,1–2%, 2–5%, 5–10%, 10–25%, 25–50%, 50–75%, 75–95%, 95–100%;Peet et al., 1998) separately in each 10 � 10 m quadrant. We usedcover class midpoints, averaged per plot for analysis. In order toquantify the understory light environment, we took a digital hemi-spherical canopy photograph using a fish-eye lens at 1 m above theground surface at the midpoint of each transect. Each photographwas manually edited to remove glare prior to analysis withWinSCANOPY version 2005a (Regent Instruments, Inc., Quebec,Canada), which was used to estimate total understory lightlevels throughout the growing season based on solar tracks (May1–September 30; moles m�2 day�1).

In four 10 � 10 m subplots within each plot, we dug a shallowpit to gather soil and measure horizon depth. Soil collection wasinclusive of the O, A, and B-horizons. Corresponding horizons fromthe four subplots were pooled for analysis. Soil samples were ana-lyzed using standard protocols at A&L Analytical Laboratories inMemphis, Tennessee. Soil pH was determined in a 1:1 soil/watersuspension. Exchangeable bases were assessed using NH4Clextraction rather than buffered NH4 acetate because of the low

FirSpruceDeciduousOther

> 10

cm

dbh

5

-10

cm d

bh

0.1-

5 cm

dbh

10

-137

cm

< 1

0 cm

Dia

met

er c

lass

H

eigh

tcla

ss

Elevation (m)< 1600

n = 121600-1750

n = 131750-1900

n = 25> 1900

n = 10

Fig. 1. Comparison of importance value of Abies fraseri, Picea rubens, and deciduousspecies across four elevation bands and five size classes.

100 S.E. Stehn et al. / Forest Ecology and Management 289 (2013) 98–105

concentrations of cations found in acidic soils. Calcium, magne-sium, potassium, and sodium concentrations were used to calcu-late percent base saturation. The ratio of exchangeable calciumto aluminum (Ca:Al; non-molar) was used as an indicator of poten-tial aluminum toxicity (Cronan and Grigal, 1995). Mean (±1 SE)Ca:Al ratios varied from 8.7 ± 1.6 (range 0.3–67.6) for the O horizonto 0.6 ± 0.1 (range 0.1–3.6) for the A horizon and 0.6 ± 0.3 (range0.1–14.3) for the B horizon. Total carbon and nitrogen were deter-mined using a LECO TruSpec carbon/nitrogen analyzer.

2.3. Data analyses

We calculated an importance value for each species in each sizeclass by averaging the relative density of each species (sum ofstems 100 m�2 per species/sum of stems 100 m�2 of all species)and frequency (# of plots with species of interest/# of plot mea-sured). For the >10 cm dbh size class, relative basal area (sum ofbasal area per species/sum of basal area of all species) replaced rel-ative density. Calculations were performed separately for each ofthe following elevation bands: <1600, 1600–1750, 1750–1900,and >1900 m.

To quantify within plot spatial variability of small regeneration(<137 cm in height), in addition to plot level estimates of regener-ation density by size class, we calculated a coefficient of variation(CV) for small regeneration density by species across the 301 � 1 m subplots contained within each 20 � 20 m plot. We evalu-ated differences in CV between species using a simple one-wayANOVA with Tukey’s pairwise comparisons. This analysis was notperformed for the other regeneration size classes because theywere only sampled in two subplots; precluding the calculation ofmeaningful within-plot CVs. We used multiple linear regressionmodels to examine trends between regeneration abundance andvariability and environmental attributes. For regression analyses,we selected independent variables that served as surrogates forgradients of soil acidity as influenced by deposition and distur-bance without introducing cross-correlations. Plot-level soil datawere used rather than modeled classes since they better describedlocal conditions relevant to plant growth and performance. As sur-rogates for soil acidity influenced by acid deposition, we used Ca:Alfor the O and A horizons (Cronan and Grigal, 1995), percent nitro-gen and percent base saturation in the O, A, and B-horizons, anddepth of the O and A-horizons. Soils in the Picea-Abies zone ofthe southern Appalachians are frequently quite shallow (Springer,1984), so it is likely that even roots of small regeneration mayreach the B-horizon. To characterize the spatial and temporalseverity of overstory disturbance, we selected easting, mean totalunderstory light per plot (mean direct and diffuse photosyntheti-cally active flux density for the growing season in moles m�2

day�1), coefficient of variation for light within each plot, live A.fraseri basal area, dead basal area, and cover of down dead woodof decay classes 1 and 2 (Jenkins et al., 2004). Easting was selectedas an estimate of time since BWA infestation, since the BWAmoved through GSMNP over roughly 20 years from the northeastto the southwest (Smith and Nicholas, 2000). Easting ranged from271,538 to 309,004 providing a suitable gradient of time sinceinfestation. We used a stepwise multiple regression procedurewith forward and backward checks (a = 0.15 to enter or exit themodel) to determine which variables were associated with regen-eration density and within-plot heterogeneity. Regression analyseswere performed with Minitab statistical software (Minitab, 1999).Because we were interested in the local variation in density wherea species occurred rather than predicting its absence, we excludedplots where the species of interest did not occur. We evaluatedassumptions of normality and constant variance using plots of stu-dentized residuals versus fitted values and normal probabilityplots. Natural log and square root transformations were used as

needed to homogenize error variance and improve model fit (Neteret al., 1996). Transformed dependent variables included A. fraseridensity, P. rubens density, deciduous density, P. rubens CV, anddeciduous species CV. Transformed independent variables in-cluded mean light, easting, deciduous density, and O-horizon per-cent nitrogen.

3. Results

3.1. Species presence and importance across size classes

Comparison of importance values by species versus elevationindicated that A. fraseri was an important component of the regen-eration layer in forests above 1600 m (Fig. 1). However, regenera-tion of this species was usually dense and patchy, as evidencedby its high mean density and standard error values in the mediumand large regeneration size classes (Table 1). Deciduous specieswere common at all elevations and were most abundant in the<10 cm diameter class (Table 1, Fig. 1). Deciduous species main-tained an importance value of P25% throughout all regenerationsize classes and elevations.

3.2. Regeneration density

Multiple regression models of A. fraseri density along environ-mental gradients suggested that indicators of soil acidity andBWA-induced disturbance were significantly associated with theabundance of A. fraseri regeneration (p < 0.001; R2 = 0.371, 0.557,and 0.384 for small, medium, and large regeneration, respectively;Table 2). Regeneration density in all size classes was associatedwith sites with a lower easting (more recently disturbed). Eleva-tion was important in determining A. fraseri density for the small(Fig. 3a) and large size classes. Medium and large A. fraseri densitywas associated with higher O-horizon nitrogen levels and lower B-horizon nitrogen levels. Density of medium size regeneration wasalso associated with deeper O-horizons.

Table 1Summary of woody vegetation plot attributes (n = 60).

Abies fraseri Picea rubens Deciduous species All tree species

Min/Max Mean ± SE Min/Max Mean ± SE Min/Max Mean ± SE Min/Max Mean ± SE

OverstoryOverstory basal area (m2 ha�1) 0/35.2 4.8 ± 1.0 0/50.0 16.0 ± 1.9 0/33.8 8.5 ± 1.0 3.2/63.6 30.8 ± 1.9Overstory density (stems ha�1) 0/1750 275.0 ± 53.6 0/675 196.7 ± 19.5 0/525 172.1 ± 17.6 125/1900 656.7 ± 53.8Mean diameter at breast height (dbh) 0/33.6 11.4 ± 1.0 0/65.3 26.7 ± 1.7 0/62.8 21.3 ± 1.5 12.6/47.7 22.8 ± 1.0Maximum dbh 0/50.3 15.8 ± 1.5 0/94.7 46.0 ± 3.0 0/88.7 36.1 ± 2.8 17.2/122.4 55.8 ± 2.7

Understory (density 100 m�2)Small regeneration (<137 cm in height) 0/2546.7 67.8 ± 42.4 0/1233.3 100.5 ± 23.8 0/3143.3 485.4 ± 82.7 3.3/3606.7 654.6 ± 99.5Medium regeneration (0.1–5 cm dbh) 0/196 20.6 ± 4.5 0/22 3.0 ± 0.5 0/38.5 9.0 ± 1.2 0/408 36.7 ± 7.1Large regeneration (5–10 cm dbh) 0/88 7.9 ± 1.8 0/14 1.4 ± 0.3 0/14 2.6 ± 0.4 0/208 13.9 ± 3.5Coefficient of variation (CV)a 1.2/5.5 3.2 ± 0.2 0.6/5.5 2.3 ± 0.1 0.5/5.5 2.0 ± 0.2 0.5/5.5 1.5 ± 0.1

a Within plot CV of stems <137 cm in height = (standard deviation between 30 1 � 1 m subplots)/mean.

Table 2Regression equations relating environmental variables to the spatial variability and density of small regeneration (<137 cm in height), and density of medium (0.1–5 cm dbh) andlarge (5–10 cm dbh) regeneration for Abies fraseri, Picea rubens, and deciduous species as a group when present. VIF = variance inflation factor.

Model equation F df R2 p-Value

VIF

Density of small regenerationln(A. fraseri density) = 13.1 + 0.00541 (elevation) � 0.000071 (easting) 12.51 39 0.371 <0.001 1.00ln(P. rubens density) = �5.78 � 0.932 ln(mean light) 6.54 50 0.118 0.014 NAln(deciduous density) = 24.8 � 18.3 (A-horizon base saturation) � 0.0363 (overstory basal area) � 0.0205 (Rhododendron spp.

cover)7.67 58 0.256 <0.001 1.00

Coefficient of variation (CV) within plots of small regenerationA. fraseri CV = 1749 � 0.748 (elevation) + 3.57 (Rubus spp. cover) � 367 (B-horizon% nitrogen) � 3.16 (O-horizon Ca:Al) 5.78 32 0.374a 0.002 1.05ln(P. rubens CV) = 4.81 + 0.267 ln(mean light) 3.02 51 0.057 0.088 NAln(deciduous CV) = �0.45 � 0.0112 (Rubus spp. cover) + 5.71 (A-horizon base saturation) 4.71 58 0.114 0.013 1.00

Density of medium regenerationln(A. fraseri density) = 455 � 6.12 (B-horizon% nitrogen) � 36.2 ln(easting) + 0.493 (O-horizon% nitrogen)2 + 0.0299 (O-horizon

depth)211.69 34 0.557 <0.001 1.20

P. rubens density = 1.91 + 0.0280 (CV of Rubus spp.) � 0.0621 (O-horizon Ca:Al) 2.45 36 0.075 0.101 1.10Sqrt(deciduous density) = 4.20 + 0.0241 (O-horizon Ca:Al) � 1.44 (O-horizon% nitrogen) + 2.41 (B-horizon% nitrogen) + 0.0251

(Rubus spp. cover)10.11 44 0.453 <0.001 1.00

Density of large regenerationln(A. fraseri density) = 4.71 � 5.31 (B-horizon% nitrogen) � 0.000056 (easting) + 0.00584 (elevation) + 1.81 (O-horizon% nitrogen) 5.99 32 0.384 0.001 1.18ln(P. rubens density) = �0.471 + 2.48 ln(O-horizon% nitrogen) � 6.12 (B-horizon% nitrogen)2 7.23 28 0.308 0.003 1.10Deciduous density = 30.3 + 0.112 (A. fraseri basal area) + 0.0599 (O-horizon Ca:Al) � 28.0 (A-horizon base saturation) 2.57 44 0.097 0.068 1.07

a Adjusted R2 provided for multiple linear regressions.

0

100

200

300

400

CV p

rese

nt(%

) Bn=52

n=60

An=41

Bn=59

Fig. 2. Mean within-plot variability for A. fraseri, P. rubens, and deciduous specieswhen present, and all tree species <137 cm tall. CV is the coefficient of variation(standard deviation/mean) of seedlings and small saplings across thirty 1 � 1 msubplots within each 20 � 20 m plot. Different letters indicate significant (a = 0.05)differences in the means of each species or species group, determined using Tukey’sSimultaneous Test of pairwise comparisons.

S.E. Stehn et al. / Forest Ecology and Management 289 (2013) 98–105 101

Multiple regression models of P. rubens regeneration were lessinformative (Table 2). Small P. rubens density was associated withlower values of understory light, though the explanatory powerwas low (R2 = 0.118). We were unable to find a significant modelfor medium size P. rubens regeneration. The model for largeP. rubens regeneration was informative (R2 = 0.308), and suggestedthat higher densities of large P. rubens were associated withsites with higher O-horizon nitrogen levels and lower B-horizonnitrogen levels (Table 2).

Regression models of deciduous regeneration density suggestedsignificant associations between regeneration density and indica-tors of acid deposition and BWA-induced disturbance (Table 2). In-creases in density of small deciduous regeneration were associatedwith sites having lower base saturation in the A-horizon, loweroverstory basal area, and lower cover of Rhododendron spp. Highermedium size deciduous density was associated with sites havinglower O-horizon nitrogen levels and higher B-horizon nitrogen lev-els, opposite the response of medium and large A. fraseri, and largeP. rubens regeneration that occurred at lower density under theseconditions. Medium size deciduous regeneration density also wasassociated with higher Rubus spp. cover. There was some evidencethat large deciduous regeneration density might be associated withhigher O-horizon Ca:Al, lower base saturation in the A-horizon,and higher A. fraseri basal areas, but the overall model was not sig-nificant (p = 0.068).

3.3. Spatial variation of small regeneration (<137 cm in height)

Within-plot spatial variation in small A. fraseri regeneration wassignificantly (p < 0.05) greater than P. rubens or deciduous specieswhen considering only plots where A. fraseri, P. rubens, and

0

100

200

300

400

500

600

020

40

6017001800

19002000

Fir C

V

O-h

orizo

n Ca

:Al

Elevation (m)

0

20

40

60

80

100

120

140

west

east1600

1700

18001900

2000

Fir

rege

nera

tion

(ste

ms

100m

-2)

Elev

atio

n (m

)

(a)

(b)

1600

Fig. 3. Change in the (a) density of A. fraseri regeneration and (b) spatial variabilityof A. fraseri regeneration <137 cm tall across gradients of elevation and easting andelevation and O-horizon Ca:Al, respectively. Note the position of the elevation axisis different on each diagram for best display. CV is the coefficient of variation(standard deviation/mean) of within plot A. fraseri regeneration <137 cm tall. In theCV model, other significant predictors Rubus spp. cover and B-horizon % nitrogenwere held constant at mean to allow 3-dimensional display.

102 S.E. Stehn et al. / Forest Ecology and Management 289 (2013) 98–105

deciduous species were present (Fig. 2). Local variability in A. fraseriregeneration was associated with lower B-horizon % nitrogenlevels, lower O-horizon Ca:Al, decreasing elevation, and greaterRubus spp. cover (Table 2, Fig. 3b). None of the environmentalvariables measured exhibited significant influence on the spatialvariability of small P. rubens regeneration. Local variability ofsmall deciduous regeneration was associated with lower Rubusspp. cover and higher base saturation in the A-horizon (Table 2).

4. Discussion

4.1. Effect of balsam woolly adelgid-induced disturbance onregeneration

Our results suggest that southern Appalachian Picea-Abies for-ests are still in a state of compositional and structural change thatvaries with time since BWA infestation. Across our sample plots,variability in the density of A. fraseri regeneration was significantlygreater than that of P. rubens or deciduous species. Based upon ourobserved densities, small A. fraseri regeneration reported in earlierstudies (Busing and Clebsch, 1988; Witter and Ragenovich, 1986;Smith and Nicholas, 2000) has advanced into taller height classes.

We also observed fewer medium-sized deciduous stems than anearlier survey (Nicholas et al., 1992), possibly due to canopy re-growth resulting in reduced regeneration of disturbance-adaptedgap colonizers such as Prunus pensylvanica (fire cherry; Marks,1974).

When considered in the context of earlier studies, our resultssuggest that regeneration of A. fraseri has spatially shifted throughtime with overstory mortality resulting from BWA, highlightingthe importance of site history in determining contemporary regen-eration patterns. We observed greater densities of A. fraseri regen-eration in the western portion of our study where infestations ofHWA were more recent. According to a 1990–91 survey conductedby Smith and Nicholas (2000), advanced regeneration of A. fraseriprogressed into taller height classes following severe overstorymortality, but densities of younger and smaller regeneration werelow due to reduced density of reproductive adults and inhospitableenvironmental conditions. A decade after overstory mortality onMount LeConte in GSMNP, Jenkins (2003) observed a 77% reduc-tion in the density of A. fraseri stems <1 cm dbh, but a 3� increasein stems 1–10 cm dbh compared to pre-adelgid conditions. In astudy conducted in contemporary forests, Johnson and Smith(2005) observed greater survival of A. fraseri seedlings in areas withpartially open canopies compared to areas with full canopy cover.However, seedling survival was zero on sites with completely opencanopies. In our study, the greater regeneration in the most re-cently infested sites was likely a mix of advanced and post-adelgidreproduction that will continue to decrease in density with standdevelopment and decreased light availability.

Because A. fraseri traditionally dominated southern Appalachianforests above 1750 m (Whittaker, 1956), BWA-induced distur-bance had a greater effect at these higher elevations, as shownby observations of increasing basal area of dead trees with increas-ing elevation (Zedaker et al., 1988; Busing and Pauley, 1994).Across our plots, we found dead basal area and understory lightto be significantly (p = 0.05) correlated with elevation (r = 0.317and 0.303 respectively). We also found that the density of smallP. rubens regeneration was associated with lower light levels, andwas more variable on sites with higher light, indicating possibleinhibition in areas with minimal canopy cover. Although highlight exposure may inhibit the growth of P. rubens regeneration(Alexander et al., 1995), high-light, open canopy environmentsencourage the establishment and persistence of other species,including many deciduous trees and Rubus species (Ricard andMessier, 1996). BWA-induced disturbance has greatly increasedthe density (Boner, 1979; Pauley and Clebsch, 1990) and variability(Jenkins, 2003) of Rubus spp. in GSMNP. Because the Rubus speciescommon in our study area generally grow in dense patches ofsingle canes up to 2 m tall, Rubus can be a significant competitor(Wilson and Shure, 1993). Density of A. fraseri regeneration(<137 cm tall) was found to be low in areas with high Rubus spp.densities (Pauley and Clebsch, 1990) and our data indicated thathigh Rubus spp. cover was also correlated with increased localvariability of A. fraseri regeneration.

4.2. Effect of soil chemistry on regeneration

Our results suggest that soil nutrient status in concert with theeffects of BWA-induced disturbance strongly influence the regen-eration dynamics in Picea-Abies forest. Soil solutions of Picea-Abiesforests are dominated by nitrate, sulfate, monomeric aluminum,and hydrogen (Johnson et al., 1992). Consequently, watershedexports of nitrates and sulfates are very high, causing the rapidexport of base cations important for plant growth in this nutrientpoor forest (Nodvin et al., 1995). We observed a positive relation-ship between the densities of medium and large A. fraseri andP. rubens regeneration and nitrogen content of the O horizon. This

S.E. Stehn et al. / Forest Ecology and Management 289 (2013) 98–105 103

relationship was not evident for small regeneration, suggestingthat increased N may facilitate the longer-term survival of coniferreproduction rather than establishment. However, O horizon Ncontent was negatively correlated with the density of deciduousspecies regeneration, which was positively correlated with greaterCa:Al ratio, suggesting that greater Ca availability is important tothe establishment and persistence of deciduous speciesreproduction.

Acid deposition and subsequent calcium loss has long beenassociated with growth decline in overstory P. rubens (e.g., Adamsand Eagar, 1992; Cook and Zedaker, 1992; Shortle et al., 1997). Inthe understory, our data suggest that O-horizon Ca:Al, an indicatorof aluminum toxicity risk to plants (Cronan and Grigal, 1995), maylimit the persistence of deciduous species reproduction and in-crease the local variability of Abies regeneration. Detected at levelsknown to inhibit cation uptake in southern Appalachian Picea-Abies forests, monomeric aluminum can reduce fine root growthin mineral soil horizons (Johnson et al., 1992). In southern Appala-chian Picea-Abies forests, atmospheric and hydrological fluxes, notbiological (i.e. litterfall) fluxes, tend to dominate abovegroundnutrient cycling (Johnson et al., 1991) and soil nutrients can varygreatly across even small spatial scales (Feldman et al., 1991).Within one 20 � 20 m plot, nutrients may shift and flow in solutionto form ‘‘hotspots’’ of nutrient availability. Greater N availabilitymay favor the persistence of A. fraseri, while the associated in-crease in cation leaching may exclude woody species regeneration.However, on sites where N enrichment increases soil solution acid-ity and the availability of Al, A. fraseri reproduction may becomemore variable in response to small-scale variations in soil solutionchemistry.

4.3. Concurrent effects of exogenous disturbances on ground-layercompetitive dynamics

BWA-induced canopy conditions were often secondary to theavailability of soil nutrients in determining variability and densityof regeneration, suggesting that interactions between acid deposi-tion and shifts in composition or structure due to the BWA bothcontribute to regeneration dynamics. Both BWA and acid deposi-tion have had major effects on Picea-Abies forest structure andgrowth over the past 30 years and have contributed to chronicstress of tree species in these forests. These two anthropogenic dis-turbances have likely altered regeneration regimes based upontheir individual and coincident effects on ecosystem function.

Woody regeneration dynamics, especially in the small sizeclass, may be strongly influenced by conditions created byground-layer vegetation. Since ground-layer vegetation responseto disturbance is spatially complex and depends on multiple gradi-ent interactions (Fahey and Puettmann, 2007), we would expectcompetition between woody and herbaceous growth forms to beequally complex. Additionally, forests low in base cation availabil-ity and susceptible to soil acidification, such as our study area, arethe most susceptible to changes in competitive plant interactionsdue to increased nitrogen availability (Bobbink et al., 1998). Aciddeposition has been shown to affect ground-layer species compo-sition through changes in light caused by overstory uptake ofadded nitrogen (van Dobben et al., 1999) and by exclusion of spe-cies through competition with nitrophilous species (Bobbink et al.,1998; Gilliam, 2006). There is some evidence for nitrogen-inducedcompetition in our study, as nitrogen hotspots may be contributingto the establishment and persistence of Rubus spp. (Stehn et al.,2011). We observed greater variability in A. fraseri regenerationwith increasing cover of this genus. Increases in soil nitrogen havebeen linked to increases in growth (Hättenschwiler and Körner,1996), abundance (Diekmann and Falkengren-Grerup, 2002), andseed germination (Jobidon, 1993) of Rubus spp. Previously linked

to the influence of BWA-induced disturbance (Pauley and Clebsch,1990), the increase in Rubus spp. cover over the past 30 years mayalso be influenced by the spatial distribution of nitrogendeposition.

We conclude that the combined effects of exogenous distur-bances may be contributing to an undermining of ecological resil-ience in Picea-Abies forests of the southern Appalachians. Wepropose that drastic BWA-induced canopy mortality and subse-quent release of suppressed regeneration, in addition to high ratesof chronic acid deposition and nitrogen-induced changes toground-layer community dynamics, have created a new patternof regeneration across Picea-Abies forests. Because the full recoveryof this imperiled ecosystem remains uncertain, the persistence ofthis forest type likely hinges on the response of regeneration tothe concurrent influences of BWA infestation and soil chemistry.In the long-term, the response of Picea-Abies forests to these con-current influences will likely occur within the context of a chang-ing climate. Predictive models have shown that both A. fraseri andP. rubens are at risk of extirpation under most climate change sce-narios (Iverson et al., 2008; Potter et al., 2010) and climate changemay alter the frequency and intensity of exogenous disturbanceswithin these forests (Dale et al., 2001).

Acknowledgments

The National Park Service-Air Resource Division, the StudentConservation Association, and the Michigan Technological Univer-sity Ecosystem Science Center provided financial support for thisstudy. We thank Becky Hylton for assistance with the initiationof the stratification protocol and original plot establishment, aswell as field assistants Thomas McDonough, Katri Morley, BrandonPotter, Nicole Samu, Jenny Stanley, Meg Walker-Milani, BettinaUhlig, and Philip White; lab assistants Jennifer Boettger, MikeFoster, Maria Parisot, Bliss Sengbusch, and Aaron Wuori; and othersupport provided by the Great Smoky Mountains National ParkDivision of Resource Management and Science staff. ChristopherSwanston and Janice Glime provided valuable input on the studyand helpful comments on earlier versions of this manuscript.

References

Adams, M.B., Eagar, C., 1992. Impacts of acidic deposition on high-elevation spruce-fir forests: results from the Spruce-Fir Research Cooperative. For. Ecol. Manage.51, 195–205.

Adams, M.B., Kochenderfer, J.N., Edwards, P.J., 2007. The Fernow Watershedacidification study: ecosystem acidification, nitrogen saturation and basecation leaching. Water Air Soil Pollut. 7, 267–273.

Alexander, J.D., Donnelly, J.R., Shane, J.B., 1995. Photosynthetic and transpirationalresponses of red spruce understory trees to light and temperature. Tree Phys.15, 393–398.

Allen, T.R., Kupfer, J.A., 2001. Spectral response and spatial pattern of Fraser firmortality and regeneration, Great Smoky Mountains. Plant Ecol. 156, 59–74.

Bengtsson, J., 2002. Disturbance and Resilience in Soil Animal Communities.Gauthier-Villars/Editions Elsevier, pp. 119–125.

Blake, L., Goulding, K.W.T., 2002. Effects of atmospheric deposition, soil pH andacidification on heavy metal contents in soils and vegetation of semi-naturalecosystems at Rothamsted Experimental Station, UK. Plant Soil 240, 235–251.

Bobbink, R., Hornung, M., Roelofs, J.G.M., 1998. The effects of air-borne nitrogenpollutants on species diversity in natural and semi-natural Europeanvegetation. J. Ecol. 86, 717–738.

Boner, R.R. 1979. Effects of Fraser Fir Death on Population Dynamics in SouthernAppalachian Boreal Ecosystems. MS Thesis, University of Tennessee, Knoxville.

Busing, R.T., Clebsch, E.E.C., 1988. Fraser fir mortality and the dynamics of a GreatSmoky Mountains fir-spruce stand. Castanea 53, 177–182.

Busing, R.T., Pauley, E.F., 1994. Mortality trends in a southern Appalachian redspruce population. For. Ecol. Manage. 64, 41–45.

Cook, E.R., Zedaker, S.M., 1992. The dendroecology of red spruce decline. In: Eagar,C., Adams, M.B. (Eds.), Ecology and Decline of Red Spruce in the Eastern UnitedStates. Springer-Verlag, New York, NY, pp. 192–231.

Cronan, C.S., Grigal, D.F., 1995. Use of calcium/aluminum ratios as indicators ofstress in forest ecosystems. J. Environ. Qual. 24, 209–226.

Dale, V.H., Joyce, L.A., McNulty, S., Neilson, R.P., Ayres, M.P., Flannigan, M.D., Hanson,P.J., Irland, L.C., Lugo, A.E., Peterson, C.J., Simberloff, D., Swanson, F.J., Stocks, B.J.,

104 S.E. Stehn et al. / Forest Ecology and Management 289 (2013) 98–105

Wotton, . Climate change and forest disturbances. BioScience 51, 723–734.Diekmann, M., Falkengren-Grerup, U., 2002. Prediction of species response to

atmospheric nitrogen deposition by means of ecological measures and lifehistory traits. J. Ecol. 90, 108–120.

Eagar, C., 1984. Review of the biology and ecology of the balsam woolly aphid insouthern Appalachian spruce-fir forests. In: White, P.S. (Ed.), The SouthernAppalachian Spruce-Fir Ecosystem: Its Biology and Threats. Uplands FieldResearch Laboratory, Gatlinburg, Tennessee, pp. 36–50.

Elias, P.E., Burger, J.A., Adams, M.B., 2009. Acid deposition effects on forestcomposition and growth on the Monongahela National Forest, West Virginia.For. Ecol. Manage. 258, 2175–2182.

Everham, E.M., Brokaw, N.V.L., 1996. Forest damage and recovery from catastrophicwind. Bot. Rev. 62, 113–185.

Fahey, R.T., Puettmann, K.J., 2007. Ground-layer disturbance and initial conditionsinfluence gap partitioning of understorey vegetation. J. Ecol. 95, 1098–1109.

Feldman, S.B., Zelazny, L.W., Baker, J.C., 1991. High-elevation forest soils of thesouthern Appalachians. 1. Distribution of parent materials and soil landscaperelationships. Soil Sci. Soc. Am. J. 55, 1629–1637.

Folke, C., Carpenter, S., Walker, B., Scheffer, M., Elmqvist, T., Gunderson, L., Holling,C.S., 2004. Regime shifts, resilience, and biodiversity in ecosystem management.Ann. Rev. Ecol. Evol. Syst 35, 557–581.

Foster, D.R., Zebryk, T., Schoonmaker, P., Lezberg, A., 1992. Postsettlement history ofhuman land-use and vegetation dynamics of a Tsuga canadensis (hemlock)woodlot in central New-England. J. Ecol. 80, 773–786.

Gilliam, F.S., 2006. Response of the herbaceous layer of forest ecosystems to excessnitrogen deposition. J. Ecol. 94, 1176–1191.

Gunderson, L.H., 2000. Ecological resilience – in theory and application. Ann. Rev.Ecol. Syst. 31, 425–439.

Hain, F.P., Arthur, F.H., 1985. The role of atmospheric deposition in the latitudinalvariation of Fraser fir mortality caused by the Balsam woolly adelgid, Adelgespiceae (Ratz.) (Hemipt., Adelgidae): A hypothesis. Zeitschrift fur AngewandteEntomologie 99, 145–152.

Hättenschwiler, S., Körner, C., 1996. Effects of elevated CO2 and increased nitrogendeposition on photosynthesis and growth of understory plants in spruce modelecosystems. Oecologia 106, 172–180.

Hollingsworth, R.G., Hain, F.P., 1991. Balsam woolly adelgid (Homoptera, Adelgidae)and spruce-fir decline in the southern Appalachians – assessing pest relevancein a damaged ecosystem. Fla Entomol. 74, 179–187.

Hollingsworth, R.G., Hain, F.P., 1994. Balsam woolly adelgid (Homoptera, Adelgidae)– effects on growth and abnormal wood productions in Fraser fir seedlings asinfluenced by seedling genetics, insect source, and soil source. Can. J. For. Res.24, 2284–2294.

Iverson, L.R., Prasad, A.M., Matthews, S.N., Peters, M., 2008. Estimating potentialhabitat for 134 eastern US tree species under six climate scenarios. For. Ecol.Manage. 254, 390–406.

Jenkins, M.A., 2003. Impact of the Balsam wooly adelgid (Adelges piceae Ratz.) on anAbies fraseri (Pursh) Poir. dominated stand near the summit of Mount LeConte.Tennessee. Castanea 68, 109–118.

Jenkins, M.A., Webster, C.R., Parker, G.R., Spetich, M.A., 2004. Coarse woody debris inmanaged central hardwood forests of Indiana. USA. For. Sci. 50, 781–792.

Jobidon, R., 1993. Nitrate fertilization stimulates emergence of red raspberry(Rubus-idaeus L.) under forest canopy. Fertil. Res. 36, 91–94.

Johnson, D.M., Smith, W.K., 2005. Refugial forests of the southern Appalachians:photosynthesis and survival in current-year Abies fraseri seedlings. Tree Phys.25, 1379–1387.

Johnson, D.W., Van Miegroet, H., Lindberg, S.E., Todd, D.E., Harrison, R.B., 1991.Nutrient cycling in red spruce forests of the Great Smoky Mountains. Can. J. For.Res. 21, 769–787.

Johnson, A.H., Friedland, A.J., Miller, E.K., Battles, J.J., Huntington, T.G., Vann, D.R.,Strimbeck, G.R., 1992. Regional evaluations of acid deposition effects on forests:eastern spruce-fir. In: Johnson, D.W., Lindberg, S.E. (Eds.), AtmosphericDeposition and Forest Nutrient Cycling. Springer-Verlag, New York, NY, pp.496–525.

Lawrence, G.B., David, M.B., Shortle, W.C., 1995. A new mechanism for calcium lossin forest-floor soils. Nature 378, 162–165.

Lee, C.E., Cox, J.M., Foster, D.M., Humphrey, H.L., Woosley, R.S., Butcher, D.J., 1997.Determination of aluminum, calcium, and magnesium in Fraser fir (Abies fraseri)foliage from five native sites by atomic absorption spectrometry: the effect ofelevation upon nutritional status. Microchem. J. 56, 236–246.

Levin, S.A., 2000. Multiple scales and the maintenance of biodiversity. Ecosystems 3,498–506.

Marks, P.L., 1974. The role of pin cherry (Prunus pensylvanica L.) in the maintenanceof stability in northern hardwood ecosystems. Ecol. Monogr. 44, 73–88.

McLaughlin, S.B., Anderson, C.P., Edwards, N.T., Roy, W.K., Layton, P.A., 1990.Seasonal patterns of photosynthesis and respiration of red spruce saplings fromtwo elevations in declining southern Appalachian stands. Can. J. For. Res. 20,485–495.

Minitab, 1999. Minitab Release 13 for Windows. Minitab, Inc., State College, PA.Neter, J., Kutner, M., Wasserman, W., Nachtsheim, C., Neter, J., 1996. Applied Linear

Statistical Models, fourth ed. McGraw-Hill/Irwin, Chicago, IL.Nicholas, N.S., Zedaker, S.M., 1989. Ice damage in spruce-fir forests of the Black

Mountains, North Carolina. Can. J. For. Res. 19, 1487–1491.Nicholas, N.S., Zedaker, S.M., Eagar, C., Bonner, F.T., 1992. Seedling recruitment and

stand regeneration in spruce-fir forests of the Great Smoky Mountains. Bull.Torrey Bot. Club 119, 289–299.

Nodvin, S.C., Van Miegroet, H., Lindberg, S.E., Nicholas, N.S., Johnson, D.W., 1995.Acidic deposition, ecosystem processes, and nitrogen saturation in a highelevation Southern Appalachian watershed. Water Air Soil Pollut. 85, 1647–1652.

Nystrom, M., Folke, C., 2001. Spatial resilience of coral reefs. Ecosystems 4, 406–417.Ohmann, J.L., Spies, T.A., 1998. Regional gradient analysis and spatial pattern of

woody plant communities of Oregon forests. Ecol. Monogr. 68, 151–182.Pardo, L.H., Duarte, N., 2007. Assessment of Effects of Acidic Deposition on Forested

Ecosystems in Great Smoky Mountains National Park Using Critical Loads forSulfur and Nitrogen. Air Resources Division, National Park Service, Lakewood,CO. p. 141.

Pauley, E.F., 1989. Does Rubus Canadensis Interfere with The Growth of Fraser FirSeedlings? MS Thesis, University of Tennessee, Knoxville, Tennessee, p. 113.

Pauley, E.F., Clebsch, E.E.C., 1990. Patterns of Abies fraseri regeneration in a greatsmoky mountains spruce-fir forest. Bull. Torrey Bot. Club 117, 375–381.

Peet, R.K., Wentworth, T.R., White, P.S., 1998. A flexible multipurpose method forrecording vegetation composition and structure. Castanea 63, 262–274.

Peterjohn, W.T., Adams, M.B., Gilliam, F.S., 1996. Symptoms of nitrogen saturationin two central Appalachian hardwood forest ecosystems. Biogeochemistry 35,507–522.

Potter, K.M., Hargrove, W.H., Koch, F.H., 2010. Predicting climate change extirpationrisks for central and southern Appalachian tree species. In: Rentch, J.S., Schuler,T.M., (Eds.), Proceedings of Conference on the Ecology and Management ofHigh-elevation Forests in the Central and Southern Appalachian Mountains. 14–15 May 2009, Slatyfork, WV. Gen. Tech. Rep. NRS-P-64. Newtown Square, PA,USDA Forest Service, Northern Research Station. pp. 179–189.

Ricard, J.P., Messier, C., 1996. Abundance, growth and allometry of red raspberry(Rubus idaeus L.) along a natural light gradient in a northern hardwood forest.For. Ecol. Manage. 81, 153–160.

Rich, R.L., Frelich, L.E., Reich, P.B., 2007. Wind-throw mortality in the southernboreal forest: effects of species, diameter and stand age. J. Ecol. 95, 1261–1273.

Robarge, W.P., Johnson, D.W., 1992. The Effects of Acidic Deposition on ForestedSoils. Academic Press, Inc., San Diego, CA.

Shaver, C.L., Tonnessen, K.A., Maniero, T.G., 1994. Clearing the air at great smokymountains national park. Ecol. Appl. 4, 690–701.

Shortle, W.C., Smith, K.T., 1988. Aluminum-induced calcium deficiency syndrome indeclining red spruce. Science 240, 1017–1018.

Shortle, W.C., Smith, K.T., Minocha, R., Lawrence, G.B., David, M.B., 1997. Acidicdeposition, cation mobilization, and biochemical indicators of stress in healthyred spruce. J. Environ. Qual. 26, 871–876.

Smith, G.F., Nicholas, N.S., 1998. Patterns of overstory composition in the fir and fir-spruce forests of the Great Smoky Mountains after balsam woolly adelgidinfestation. Am. Midl. Nat. 139, 340–352.

Smith, G.F., Nicholas, N.S., 2000. Size- and age-class distributions of Fraser firfollowing balsam wooly adelgid infestation. Can. J. For. Res. 30, 948–957.

Speers, C.F., 1958. The balsam woolly adelgid in the Southeast. J. For. 56, 515–516.

Springer, M.E., 1984. Soils in the Spruce-Fir Region of the Great Smoky Mountains.The southern Appalachian Spruce-Fir Ecosystem: Its Biology and Threats.Uplands Field Research Laboratory, Gatlinburg, Tennessee, pp. 201–210.

Stehn, S.E., Webster, C.R., Jenkins, M.A., Jose, S., 2011. High-elevation ground-layerplant community composition across environmental gradients in spruce-firforests. Ecol. Res. 26, 1089–1101.

van Dobben, H.F., ter Braak, C.J.F., Dirkse, G.M., 1999. Undergrowth as a biomonitorfor deposition of nitrogen and acidity in pine forest. For. Ecol. Manage. 114, 83–95.

Watmough, S.A., Aherne, J., Alewell, C., Arp, P., Bailey, S., Clair, T., Dillon, P.,Duchesne, L., Eimers, C., Fernandez, I., Foster, N., Larssen, T., Miller, E., Mitchell,M., Page, S., 2005. Sulphate, nitrogen and base cation budgets at 21 forestedcatchments in Canada, the United States and Europe. Environ. Monit. Assess.109, 1–36.

Weathers, K.C., Simkin, S.M., Lovett, G.M., Lindberg, S.E., 2006. Empirical modelingof atmospheric deposition in mountainous landscapes. Ecol. Appl. 16, 1590–1607.

White, P.S., 1984a. The Southern Appalachian Spruce-Fir Ecosystem, AnIntroduction. The southern Appalachian Spruce-Fir Ecosystem: Its Biology andThreats. Uplands Field Research Laboratory, Gatlinburg, Tennessee, pp. 1–21.

White, P.S., 1984b. The Southern Appalachian Spruce-Fir Ecosystem: Its Biology andThreats. U.S. Department of the Interior, National Park Service, p. 268.

White, R.D., Patterson, K.D., Weakley, A., Ulrey, C.J., Drake, J., 2003. VegetationClassification of Great Smoky Mountains National Park. Report Submitted toBRD-NPS Vegetation Mapping Program. NatureServe, Durham, NC, p. 376.

Whittaker, R.H., 1956. Vegetation of the Great Smoky Mountains. Ecol. Monogr. 26,1–80.

Wilson, A.D., Shure, D.J., 1993. Plant competition and nutrient limitation duringearly succession in the southern Appalachian mountains. Am. Midl. Nat. 129, 1–9.

Witter, J.A., Ragenovich, I.R., 1986. Regeneration of Fraser fir at Mt. Mitchell, NorthCarolina, after depredations by the balsam woolly adelgid. For. Sci. 32, 585–594.

Zaccherio, M.T., Finzi, A.C., 2007. Atmospheric deposition may affect northernhardwood forest composition by altering soil nutrient supply. Ecol. Appl. 17,1929–1941.

Zedaker, S.M., Nicholas, N.S., Eagar, C., White, P.S., Burk, T.E., 1988. Standcharacteristics associated with potential decline of spruce-fir forests in the

S.E. Stehn et al. / Forest Ecology and Management 289 (2013) 98–105 105

southern Appalachians. In: Proceedings of the US/FRG Research Symposium:Effects of Atmospheric Pollutants on the Spruce-Fir Forests of the Eastern USand the Federal Republic of Germany. USDA Forest Service, Washington, DC, pp.123–131.

Zvereva, E.L., Kozlov, M.V., 2001. Effects of pollution-induced habitat disturbance onthe response of willows to simulated herbivory. J. Ecol. 89, 21–30.